Retinal oxygen supply shaped the functional evolution of the vertebrate eye

Abstract

The retina has a very high energy demand but lacks an internal blood supply in most vertebrates. Here we explore the hypothesis that oxygen diffusion limited the evolution of retinal morphology by reconstructing the evolution of retinal thickness and the various mechanisms for retinal oxygen supply, including capillarization and acid-induced haemoglobin oxygen unloading. We show that a common ancestor of bony fishes likely had a thin retina without additional retinal oxygen supply mechanisms and that three different types of retinal capillaries were gained and lost independently multiple times during the radiation of vertebrates, and that these were invariably associated with parallel changes in retinal thickness. Since retinal thickness confers multiple advantages to vision, we propose that insufficient retinal oxygen supply constrained the functional evolution of the eye in early vertebrates, and that recurrent origins of additional retinal oxygen supply mechanisms facilitated the phenotypic evolution of improved functional eye morphology.

A novel acidification mechanism for greatly enhanced oxygen supply to the fish retina

“…First, we confirmed the previous descriptions of a choroid rete mirabile and high PO 2 in the eye of rainbow trout ( Oncorhynchus mykiss , Walbaum, 1792) and to compare the retinal PO 2 values to those of white sturgeon ( Acipenser transmontanus , Richardson, 1836) that is not expected to possess a choroid rete mirabile based on the absence of this structure in other members of the genus ( Berenbrink et al, 2005 ; Damsgaard et al, 2019 ). Histological sectioning of both species' eyes confirmed the presence of a choroid rete mirabile in rainbow trout and its absence in white sturgeon ( Figure 1AB ).…”

“…Using published data ( Damsgaard et al, 2019 ), we compared the morphology of the inner and outer retina in species with and without a choroid rete mirabile ( Figure 6 ). This analysis showed significantly thicker inner retina in species with a choroid rete mirabile (204 ± 92.6 µm [mean ± s.d.…”

“… The transverse thickness of the inner- ( A ) and outer retina ( B ) in species with (red) and without (black) a choroid rete mirabile. Each dot represents species mean values obtained from the literature ( Damsgaard et al, 2019 ). Effect sizes are visualized in the upper panels, showing the observed F-statistics (black vertical line) compared to a grey null-distributions of F-statistics from a phylogenetic analysis of variance simulation.…”

“… The transverse thickness in micrometer of the seven retinal layers in species with (red) and without (black) a choroid rete mirabile: ( A ) pigment epithelium and photoreceptor layer (PEPRL), ( B ) outer nuclear layer (ONL), ( C ) outer plexiform layer (OPL), ( D ) inner nuclear layer (INL), ( E ) inner plexiform layer (IPL), ( F ) ganglion cell layer (GCL), and ( G ) nerve fiber layer (NFL). Each dot represents species mean values obtained from the literature ( Damsgaard et al, 2019 ). P-values indicate the probability of the observed F-statistics lying within a null-distributions of F-statistics from a phylogenetic analysis of variance simulation.…”

“…To support such a high O 2 demand, most tissues possess a dense network of capillaries that minimize diffusion distances, facilitating the transfer of O 2 from the red blood cells (RBCs) to the respiring mitochondria. However, pigmented RBCs in capillaries on the vitreous side of the retina scatter incoming light and absorb photons before they reach the photoreceptors ( Buttery et al, 1991 ; Chase, 1982 ; Country, 2017 ; Damsgaard et al, 2019 ; Yu and Cringle, 2001 ). The result may be an impairment of visual acuity, which may explain why only the choroidal vessels lining the back of the retina (also called the choriocapillaris) perfuse the retinae of most vertebrates ( Country, 2017 ) (see Figure 1 for retinal anatomy).…”